A systems biology view of wood formation in Eucalyptus grandis trees submitted to different potassium and water regimes

Abstract

Summary Wood production in fast‐growing Eucalyptus grandis trees is highly dependent on both potassium (K) fertilization and water availability but the molecular processes underlying wood formation in response to the combined effects of these two limiting factors remain unknown. E. grandis trees were submitted to four combinations of K‐fertilization and water supply. Weighted gene co‐expression network analysis and MixOmics‐based co‐regulation networks were used to integrate xylem transcriptome, metabolome and complex wood traits. Functional characterization of a candidate gene was performed in transgenic E. grandis hairy roots. This integrated network‐based approach enabled us to identify meaningful biological processes and regulators impacted by K‐fertilization and/or water limitation. It revealed that modules of co‐regulated genes and metabolites strongly correlated to wood complex traits are in the heart of a complex trade‐off between biomass production and stress responses. Nested in these modules, potential new cell‐wall regulators were identified, as further confirmed by the functional characterization of EgMYB137. These findings provide new insights into the regulatory mechanisms of wood formation under stressful conditions, pointing out both known and new regulators co‐opted by K‐fertilization and/or water limitation that may potentially promote adaptive wood traits.

Network Analysis Combining Proteomics and Metabolomics Reveals New Insights Into Early Responses of Eucalyptus grandis During Rust Infection

“…Envisioning new strategies for enhancing plant disease resistance, one of the principal purposes of plant-pathogen studies is to understand how plants modulate genes, transcripts, proteins and metabolites to physiologically adapt and respond to pathogen invasion. Hence, researchers have used network analyses to group co-expressed genes, integrate omics datasets and reveal new insights into plant physiology (Walley et al, 2013;Ployet et al, 2019), as well as plant response to stress (El-Sharkawy et al, 2015;Yuan et al, 2018;Budzinski et al, 2019;Song et al, 2019).…”

Identification and functional evaluation of accessible chromatin associated with wood formation in Eucalyptus grandis

“…Hypergeometric tests of genes in each network were conducted with respect to xylogenesis‐related dataset enrichment. Four E. grandis xylogenesis‐related datasets were considered, namely 1597 genes associated with 13 complex wood property traits from a network‐based systems genetics study (Dataset S1 from Mizrachi et al ., ), a curated list of 542 E. grandis homologues of SCW‐related reference genes (Dataset S2 from Mizrachi et al ., ), 1047 genes across three co‐expression modules (PC3, MC3, MC5) from a xylem organellar carbon allocation study with significant enrichment for SCW‐related terms (Pinard et al ., ), and 377 genes across six co‐expression modules (M1–M6) from an abiotic stress‐related xylem systems biology study that were enriched for xylogenesis‐related terms and significantly correlated with woody traits such as vessel density, vessel diameter and saccharification yield (Ployet et al ., ). A set of 363 genes across six non‐xylogenesis‐related co‐expression modules for the latter study (M7–M12) was used as a negative control for specific enrichment for xylogenesis.…”

“…Although there is some evidence that several TFs within the Arabidopsis network are functionally conserved in woody plants (Zhong et al ., , ; Kalluri et al ., ; Nakano et al ., ), the presence of woody plant‐specific subgroups of MYB TFs with proven roles in regulating xylem development (Soler et al ., , ) and a large number of novel protein–DNA interactions in model woody plants (Chen et al ., ) suggests that SCW transcriptional networks undergo rewiring in different lineages. Systems genetics and co‐expression network analyses in Eucalyptus , which is emerging as an important model for wood formation, are implicating new genes in certain aspects of wood formation or linking them to lignocellulosic biomass traits (Myburg et al ., ; Dharanishanthi & Dasgupta, ; Mizrachi et al ., ; Pinard et al ., ; Ployet et al ., ). However, the mechanisms by which they are transcriptionally regulated through interactions with CREs in the context of accessible chromatin in developing xylem is not yet understood.…”

An introduction to a Virtual Issue on Wood Biology

“…Ployet and colleagues manipulated potassium and water availability in Eucalyptus plantations: potassium depletion and water stress both negatively impacted cell expansion during wood formation. Data were integrated in a gene co‐expression framework from metabolome wood traits in order to understand the complex outcomes of these treatments on development (Ployet et al ., ). Interesting findings from this study included the identification of co‐expressed genes associated with the trade‐off between stress response and growth.…”